Coupling between annual and ENSO timescales in the malaria-climate association in Colombia.

We present evidence that the El Niño phenomenon intensifies the annual cycle of malaria cases for Plasmodium vivax and Plasmodium falciparum in endemic areas of Colombia as a consequence of concomitant anomalies in the normal annual cycle of temperature and precipitation. We used simultaneous analyses of both variables at both timescales, as well as correlation and power spectral analyses of detailed spatial (municipal) and temporal (monthly) records. During "normal years," endemic malaria in rural Colombia exhibits a clear-cut "normal" annual cycle, which is tightly associated with prevalent climatic conditions, mainly mean temperature, precipitation, dew point, and river discharges. During historical El Niño events (interannual time scale), the timing of malaria outbreaks does not change from the annual cycle, but the number of cases intensifies. Such anomalies are associated with a consistent pattern of hydrological and climatic anomalies: increase in mean temperature, decrease in precipitation, increase in dew point, and decrease in river discharges, all of which favor malaria transmission. Such coupling explains why the effect appears stronger and more persistent during the second half of El Niño's year (0), and during the first half of the year (+1). We illustrate this finding with data for diverse localities in Buenaventura (on the Pacific coast) and Caucasia (along the Cauca river floodplain), but conclusions have been found valid for multiple localities throughout endemic regions of Colombia. The identified coupling between annual and interannual timescales in the climate-malaria system shed new light toward understanding the exact linkages between environmental, entomological, and epidemiological factors conductive to malaria outbreaks, and also imposes the coupling of those timescales in public health intervention programs.

Phlebotomine sandflies and leishmaniasis risks in Colombian coffee plantations under two systems of cultivation.

The phlebotomine sandfly fauna of traditional (shaded) and intensified (unshaded) coffee plantations in Colombia was sampled by a variety of methods and the species composition and density under the two systems compared. Twenty species of Lutzomyia sandflies (Diptera: Psychodidae: Phlebotominae) were collected, of which eight were found only in the 'Coffee Axis' ('Eje Cafetero') of the departments of Caldas, Risaralda and Quindio, six were exclusive to the department of Norte de Santander and six occurred in both regions. Four species were collected only in traditional plantations and two exclusively in intensified ones. At least 13 species occurred in both plantation types. Fifteen species are opportunistic man-biters and eight are suspected vectors of leishmaniasis caused by Le. braziliensis, Le. panamensis or Le. mexicana. Seven species were collected inside houses and may be involved in intradomiciliary transmission of Leishmania. The dominant species in Norte de Santander was Lu. spinicrassa, which made up 93.8% of all the sandflies collected in this department. This species was absent from the Eje Cafetero and a number of others among the 15 recorded there might be responsible for Leishmania transmission in this region, including Lu. trapidoi, Lu. yuilli, Lu. gomezi, L. hartmanni and Lu. ovallesi. Sandfly population densities were significantly higher in traditional plantations than in intensified ones. Residents of traditional plantations were able to describe sandflies in significantly more detail than those of intensified plantations, based on seven basic characteristics related to the appearance and biting behaviour of the insects.

Diversion of Anopheles gambiae from children to other hosts following exposure to permethrin-treated bednets.

Permethrin-treated bednets reduce mortality and morbidity from malaria in Gambian children. However, it is not certain how this effect is achieved, as neither mosquito numbers nor the human blood index of indoor-resting female Anopheles gambiae Giles sensu lato (Diptera: Culicidae) mosquitoes have been reduced when treated bednets were introduced into a community. One possibility is that insecticide-treated bednets divert mosquitoes from children to adults. To investigate this hypothesis, a cross-over trial with insecticide-treated bednets was undertaken in two small Gambian villages. To differentiate mosquitoes that had fed on children from those that had fed on adults, all children in the study villages were immunized with rabies vaccine before the trial. Using the detection of rabies antibody in a bloodmeal as an indicator that a mosquito had bitten a child, it was found that the percentage of blood-fed mosquitoes caught indoors that had bitten a child fell significantly from 30.8% to 9.2% and from 28.0% to 6.9% in each village after insecticide-treated bednets were introduced. To investigate the possibility that some diversion to animals had occurred, a PCR analysis for human beta-globin DNA was undertaken on selected samples. The results of this investigation were confusing, as some rabies-antibody positive bloodmeals were negative for human DNA. This may have been due to cross-reacting antibodies in animal sera and/or DNA degradation by digestion in the mosquito. Although good evidence for diversion of mosquitoes away from children was obtained, it remains uncertain whether diversion was mainly to adult humans, to animals or to both.

Permethrin-treated bed nets do not have a 'mass-killing effect' on village populations of Anopheles gambiae s.l. in The Gambia.

In The Gambia, the use of permethrin-treated bed nets has led to a reduction in morbidity and mortality from malaria in children. However, no clear evidence has been found for a 'mass-killing effect' on the mosquito vectors as a result of this intervention. Two further entomological studies to investigate this phenomenon have been carried out. In one study, 20 villages were paired so that bed nets in one member of each pair were treated with permethrin. In the other, a cross-over design was used in which treated and untreated bed nets were exchanged between 2 villages. Longevity, biting rate and resting density of the malaria vector population and sporozoite rates were assessed in both studies. Malaria vectors were equally abundant and long-lived, and as likely to be infective, in villages with treated bed nets as in those with untreated nets. However, a clear reduction in the density of the indoor-resting population of mosquitoes in rooms with treated bed nets was found, probably reflecting the excito-repellency of the insecticide. This study confirmed that, in The Gambia, the protection against death and morbidity from malaria seen in children using treated bed nets must be due primarily to personal protection rather than to a 'mass-killing effect' on the mosquito vector population at a village level.

Anopheles gambiae gonotrophic cycle duration, biting and exiting behaviour unaffected by permethrin-impregnated bednets in The Gambia.

Permethrin-impregnated bednets protect children against malaria in The Gambia, where Anopheles gambiae complex mosquitoes are the main vectors of malaria. However, no effect has been found on mosquito density, parous rates or sporozoite rates in An.gambiae sensu lato populations; only a reduction in the numbers of mosquitoes resting indoors in rooms with treated bednets. A possible explanation for this paradox is that exposure to treated bednets leads to changed vector behaviour such as a shift in biting time, a diversion to biting outdoors instead of indoors, to biting animals instead of humans, or to increased duration of the gonotrophic cycle. To investigate these possibilities, we observed the biting and existing behaviour of An.gambiae in ten pairs of villages, in half of which the residents used permethrin-treated bednets. The possible influence of treated bednets on the gonotrophic cycle length was evaluated by mark-release-recapture experiment. No significant difference was found between villages with treated and untreated bednets in the indoor/outdoor ratio of human biting, in mean biting times or in human blood indices of An.gambiae females found resting indoors in the mornings. The proportions of unfed, fed or gravid An.gambiae females collected in exit traps, and the number of females exiting showed no significant differences between rooms with treated and untreated bednets. Indications for a gonotrophic cycle length of 2 days were found. No evidence for any change in duration of the gonotrophic cycle in relation to exposure to treated bednets was found, although the number of recaptures was low in the villages with treated bednets. Since equal numbers of infective An.gambiae were found in villages with treated or untreated bednets, and no changes in mosquito behaviour were detected, we cannot account for how children are protected against malaria by treated bednets. One possibility is that mosquitoes divert to bite other hosts, including adults.

Movement of Anopheles gambiae s.l. malaria vectors between villages in The Gambia.

Movement of mosquitoes belonging to the Anopheles gambiae complex (mixed wild populations of An.arabiensis, An.gambiae and An.melas) between three neighbouring rural villages in The Gambia was investigated by mark-release-recapture. A total of 12,872 mosquitoes were collected in bednets, marked with a magenta fluorescent powder and released over a 15-day period in one of the villages. A further 15,507 mosquitoes were collected in exit traps, marked with a yellow powder and released over the same period. Mosquitoes were captured daily in all three villages using pyrethrum spray catches, as well as bednet and exit trap catches. The catching period extended for 6 days after the last day of release. Of the mosquitoes released, 372 (1.3%) were recaptured 2-21 days later. Of these recaptures, 272 were caught in the release village, and 98 were caught in other villages situated 1-1.4 km away. The 'movement index' between villages was calculated as 17.2% (12.2-22.4% confidence limits) for mosquitoes released after feeding and 20.1% (14.7-25.3%) for those released unfed. These results suggest that movement of mosquitoes between neighbouring villages in The Gambia seriously affects the entomological evaluation of pyrethroid-impregnated bednet programmes in areas where treated and untreated villages are interspersed.

Indoor resting heights of some anophelines in Colombia.

The nocturnal, indoor resting behavior of female anophelines in Colombia was studied. Anopheles darlingi and An. marajoara had a tendency to rest close to the ground, but An. oswaldoi and An. rangeli rested higher up. This behavior was independent of bloodfed status (except for An. oswaldoi) and whether the surface had been sprayed with DDT. With this information it should be possible to modify insecticide applications to coincide with the resting preferences of these species.

First record of DDT resistance in Anopheles darlingi.

DDT susceptibility of Anopheles darlingi was compared from the southeastern and northwestern regions of Colombia. Mosquitoes from southeastern Colombia (Puerto Lleras) were fully susceptible to DDT but in the northwest (Quibdo) LT50s were 14.3 times higher. This resistance appeared to be restricted to the Quibdo area. This is the first time that the DDT resistance has been detected in this important malaria vector.

Irritability to DDT of natural populations of the primary malaria vectors in Colombia.

Natural populations of Anopheles albimanus, An. darlingi and An. nuneztovari were tested for their irritability to DDT in different regions of Colombia. Individual anophelines were exposed to filter papers impregnated with 2% DDT and irritability was determined based on the number of flights a mosquito made in 15 min. All three species showed variability in their irritability to DDT. Anopheles albimanus showed irritability only in Bolivar, but not in three other regions. Anopheles darlingi showed no irritability in neither the Atlantico nor Llanos regions, while An. nuneztovari showed irritability in the Oriente but not in Uraba. The irritability to DDT shown in some populations of An. albimanus and An. nuneztovari may reduce the effectiveness of residual applications of this insecticide by causing the mosquitoes to seek untreated surfaces and/or leave the house to rest outdoors and thus avoid a lethal dose.